Abstract
Herbivorous thrips are considered as one of the most economically important pests worldwide. They cause direct damage by feeding on plants of at least 60 families including many vegetable and ornamental crops, and indirect damage by transferring devastating plant viruses. Their high and parthenogenetic reproductive capacity and hidden lifestyle (pupation
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in the soil, thigmotactic behavior) make thrips hard to control. Current pest management control relies mainly on the use of chemical pesticides, to which thrips can develop resistance. Exploiting the natural defense mechanisms of plants against thrips can provide the opportunity towards more sustainable resistance breeding. The major aim of this PhD research was to explore the molecular mechanisms underlying natural defenses of the model plant Arabidopsis thaliana (Arabidopsis) in response to the Western flower thrips (Frankliniella occidentalis). To achieve this, several non-destructive bioassays were designed to assess thrips performance on single Arabidopsis leaves or whole plants. Using RNA-sequencing in a high-density time series, combined with bioinformatic analyses, we were able to capture the transcriptional dynamics and chronology of genes within the gene regulatory network that were induced in single Arabidopsis leaves upon thrips infestation. We confirmed that jasmonic acid (JA) is the predominant phytohormone modulating the induced defense response against thrips as (1) most up-regulated genes showed an overrepresentation of bHLH TF binding motifs which correlated with the activation of JA-associated processes, (2) JA-insensitive mutant coi1-34 and the MYC triple mutant myc2,3,4 showed significantly more feeding damage and a higher number of oviposited eggs compared to the Col-0 wild-type and (3) the novel regulators discovered in the thrips-induced gene regulatory network (GRN), although having distinct roles in the thrips-GRN, are closely connected to the JA pathway. However, depending on the thrips developmental stage, the predominant JA-induced response is modulated differently. For example, L1 larvae induced a relatively higher expression level of the ethylene (ET)-coregulated JA-inducible ERF-branch marker gene PDF1.2, which correlated with defense repression, while the older developmental larval stages activated higher levels of the abscisic acid (ABA)-coregulated JA-inducible MYC-branch marker gene VSP2, which was associated with enhanced plant resistance. Interestingly, although herbivory by L2 stage larvae of thrips mainly activated the expression of the MYC-branch marker gene VSP2 in the locally infested leaves, the ERF-branch marker gene PDF1.2 was mainly activated in the systemic, undamaged leaves of Arabidopsis, which correlated with enhanced preference of subsequently attacking thrips for the youngest systemic leaf tissue. In contrast, the tissue-chewing caterpillar Mamestra brassicae induced relatively higher levels of VSP2 in the local as well as the systemic, undamaged leaves of Arabidopsis, which was associated with enhanced deterrence of subsequently attacking thrips. Collectively, the work described in this thesis provides a better understanding of thrips-induced plant defense responses, which can facilitate the development of more sustainable thrips-resistance breeding.
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